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  1. Venom is a key adaptive innovation in snakes, and how nonvenom genes were co-opted to become part of the toxin arsenal is a significant evolutionary question. While this process has been investigated through the phylogenetic reconstruction of toxin sequences, evidence provided by the genomic context of toxin genes remains less explored. To investigate the process of toxin recruitment, we sequenced the genome ofBothrops jararaca, a clinically relevant pitviper. In addition to producing a road map with canonical structures of genes encoding 12 toxin families, we inferred most of the ancestral genes for their loci. We found evidence that 1) snake venom metalloproteinases (SVMPs) and phospholipases A2(PLA2) have expanded in genomic proximity to their nonvenomous ancestors; 2) serine proteinases arose by co-opting a local gene that also gave rise to lizard gilatoxins and then expanded; 3) the bradykinin-potentiating peptides originated from a C-type natriuretic peptide gene backbone; and 4) VEGF-F was co-opted from a PGF-like gene and not from VEGF-A. We evaluated two scenarios for the original recruitment of nontoxin genes for snake venom: 1) in locus ancestral gene duplication and 2) in locus ancestral gene direct co-option. The first explains the origins of two important toxins (SVMP and PLA2), whilemore »the second explains the emergence of a greater number of venom components. Overall, our results support the idea of a locally assembled venom arsenal in which the most clinically relevant toxin families expanded through posterior gene duplications, regardless of whether they originated by duplication or gene co-option.

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  2. The role of natural selection in the evolution of trait complexity can be characterized by testing hypothesized links between complex forms and their functions across species. Predatory venoms are composed of multiple proteins that collectively function to incapacitate prey. Venom complexity fluctuates over evolutionary timescales, with apparent increases and decreases in complexity, and yet the causes of this variation are unclear. We tested alternative hypotheses linking venom complexity and ecological sources of selection from diet in the largest clade of front-fanged venomous snakes in North America: the rattlesnakes, copperheads, cantils, and cottonmouths. We generated independent transcriptomic and proteomic measures of venom complexity and collated several natural history studies to quantify dietary variation. We then constructed genome-scale phylogenies for these snakes for comparative analyses. Strikingly, prey phylogenetic diversity was more strongly correlated to venom complexity than was overall prey species diversity, specifically implicating prey species’ divergence, rather than the number of lineages alone, in the evolution of complexity. Prey phylogenetic diversity further predicted transcriptomic complexity of three of the four largest gene families in viper venom, showing that complexity evolution is a concerted response among many independent gene families. We suggest that the phylogenetic diversity of prey measures functionally relevant divergencemore »in the targets of venom, a claim supported by sequence diversity in the coagulation cascade targets of venom. Our results support the general concept that the diversity of species in an ecological community is more important than their overall number in determining evolutionary patterns in predator trait complexity.

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  3. An important goal of conservation genetics is to determine if the viability of small populations has been compromised by genetic drift leading to loss of adaptive variation. Here, we assessed the impact of drift and selection on direct measures of adaptive variation (toxin loci encoding venom proteins) in the Eastern Massasauga rattlesnake (Sistrurus catenatus), a threatened snake that exists in small populations. We estimated levels of individual polymorphism in 46 toxin loci and 1467 control loci across 12 populations of this species, and compared the results with patterns of selection on the same loci following speciation of S. catenatus and its closest relative, the Western Massasauga (S. tergeminus). Multiple lines of evidence suggest that both drift and selection have had observable impacts on standing adaptive variation. In support of drift effects, we found little evidence for selection on toxin variation within populations and a significant positive relationship between current levels of adaptive variation and long-term and short-term estimates of effective population size. However, we also observed levels of directional selection on toxin loci among populations that are broadly similar to patterns predicted from interspecific selection analyses that predate the effects of recent drift, and that functional variation in these locimore »persists despite small short-term effective sizes. We suggest that much of the adaptive variation present in populations may represent an example of “drift debt,” a non-equilibrium state where present-day measures overestimate the amount of functional genetic diversity that will be present in these populations in the future.« less
  4. Identifying the environmental correlates of divergence in functional traits between populations can provide insights into the evolutionary mechanisms that generate local adaptation. Here, we assess patterns of population differentiation in expressed venom proteins in Northern Pacific rattlesnakes (Crotalus oreganus) from 13 locations across California. We evaluate the relative importance of major biotic (prey species community composition), abiotic (temperature, precipitation, and elevation) and genetic factors (genetic distance based on RADseq loci) as correlates of population divergence in venom phenotypes. We found that over half of the variation in venom composition is associated with among-population differentiation for genetic and environmental variables, and that this variation occurred along axes defining previously observed functional trade-offs between venom proteins that have neurotoxic, myotoxic and hemorrhagic effects. Surprisingly, genetic differentiation among populations was the best predictor of venom divergence, accounting for 46% of overall variation, whereas differences in prey community composition and abiotic factors explained smaller amounts of variation (23% and 19%, respectively). The association between genetic differentiation and venom composition could be due to an isolation-by-distance effect or, more likely, an isolation-by-environment effect where selection against recent migrants is strong, producing a correlation between neutral genetic differentiation and venom differentiation. Our findings suggest that evenmore »coarse estimates of prey community composition can be useful in understanding the selection pressures acting on patterns of venom protein expression. Additionally, our results suggest that factors other than adaptation to spatial variation in prey need to be considered when explaining population divergence in venom.« less
  5. Understanding the molecular mechanisms that underlie snake venom variability provides important clues for understanding how the biological functions of this powerful toxic arsenal evolve. Here we analyzed in detail individual transcripts and venom protein isoforms produced by five specimens of a venomous snake (Bothrops atrox) from two nearby but genetically distinct populations from the Brazilian Amazon rainforest showing functional similarities in venom properties. Individual variation was observed among the venoms of these specimens, but the overall abundance of each general toxin family was conserved both in transcripts and in venom protein levels. However, when expression of independent paralogues was analyzed, remarkable differences were observed within and among each toxin group both between individuals and between populations. Transcripts for functionally essential venom proteins (“housekeeping” proteins) are highly expressed in all specimens and show similar transcription/translation rates. In contrast, other paralogues show lower expression levels and the toxins they code for vary among different individuals. These results provide support for the idea that that expression and translational differences play a greater role in defining adaptive variation in venom phenotypes than does sequence variation in protein coding genes and that convergent adaptive venom phenotypes can be generated through different molecular mechanisms.
  6. Identifying the evolutionary and ecological mechanisms that drive lineage diversification in the species-rich tropics is of broad interest to evolutionary biologists. Here, we use phylogeographic and demographic analyses of genomic scale RADseq data to assess the impact of a large geographic feature, the Amazon River, on lineage formation in a venomous pitviper, Bothrops atrox. We compared genetic differentiation in samples from four sites near Santarem, Brazil that spanned the Amazon and represented major habitat types. A species delimitation analysis identified each population as a distinct evolutionary lineage while a species tree analysis with populations as taxa revealed a phylogenetic tree consistent with dispersal across the Amazon from north to south. Phylogenetic analyses of mtDNA variation confirmed this pattern and suggest that all lineages originated during the mid- to late-Pleistocene. Historical demographic analyses support a population model of lineage formation through isolation between lineages with low ongoing migration between large populations and reject a model of differentiation through isolation by distance alone. Our results provide a rare example of a phylogeographic pattern demonstrating dispersal over evolutionary time scales across a large tropical river and suggest a role for the Amazon River as a driver of in-situ divergence by both impeding (butmore »not preventing) gene flow and through parapatric differentiation along an ecological gradient.« less